The role of fruit heteromorphism in the naturalization of Asteraceae

. 2019 Jun 24 ; 123 (6) : 1043-1052.

Jazyk angličtina Země Anglie, Velká Británie Médium print

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid30715141

Grantová podpora
I 3757 Austrian Science Fund FWF - Austria

BACKGROUND AND AIMS: Fruit heteromorphism is considered to be a bet-hedging strategy to cope with spatially or temporally heterogeneous environments. The different behaviours of the fruit morphs of the same species might also be beneficial during naturalization, once the species has been introduced to a new range. Yet, no study to date has tested the association between fruit heteromorphism and global-scale naturalization success for a large set of plant species. METHODS: We compiled two large datasets on fruit heteromorphism in Asteraceae. One dataset was on native species in Central Europe (n = 321) and the other was on species frequently planted as ornamentals (n = 584). Using phylogenetic linear and logistic regressions, we tested whether heteromorphic species are more likely to naturalize outside their native range, and in more regions of the world than monomorphic species. We also tested whether the effect of heteromorphism is modulated by life history and height of the species. KEY RESULTS: We show that heteromorphic species were more likely to naturalize outside their native range. However, among the naturalized species, heteromorphic and monomorphic species did not differ in the number of world regions where they became naturalized. A short life span and tall stature both promoted naturalization success and, when life history and height were included in the models, the effect of fruit heteromorphism on the ability to naturalize became non-significant. Nevertheless, among tall plants, heteromorphic ornamental species were significantly more likely to become naturalized in general and in more regions than monomorphic species. CONCLUSIONS: Our results provide evidence that in Asteraceae the production of heteromorphic fruits is associated with naturalization success. It appears, however, that not fruit heteromorphism per se, but a successful combination of other biological traits in fruit heteromorphic species, namely short life span and tall stature, contributes to their naturalization success.

Zobrazit více v PubMed

Blackburn TM, Pyšek P, Bacher S, et al. . 2011. A proposed unified framework for biological invasions. Trends in Ecology and Evolution 26: 333–339. PubMed

Bradley BA, Blumenthal DM, Grosholz ED, Lawler JJ. 2012. Global change, global trade, and the next wave of plant invasions. Frontiers in Ecology and the Environment 10: 20–28.

Brändel M. 2007. Ecology of achene dimorphism in Leontodon saxatilis. Annals of Botany 100: 1189–1197. PubMed PMC

Canavan S, Meyerson LA, Packer JG, et al. . 2018. Tall-statured grasses: a useful functional group for invasion science. Biological Invasions. doi: 10.1007/s10530-018-1815-z. DOI

Cheptou P-O, Carrue O, Rouifed S, Cantarel A. 2008. Rapid evolution of seed dispersal in an urban environment in the weed Crepis sancta. Proceedings of the National Academy of Sciences, USA 105: 3796–3799. PubMed PMC

Cullen J, Knees SG, Cubey HS (eds). 2011. The European garden flora. Flowering plants: a manual for the identification of plants cultivated in Europe, both out-of-doors and under glass. Cambridge/New York: Cambridge University Press.

Danihelka J, Chrtek J, Kaplan Z. 2012. Checklist of vascular plants of the Czech Republic. Preslia 84: 647–811.

Dehnen-Schmutz K, Touza J, Perrings C, Williamson M. 2007. The horticultural trade and ornamental plant invasions in Britain. Conservation Biology 21: 224–231. PubMed

Doudová J, Douda J, Mandák B. 2017. The complexity underlying invasiveness precludes the identification of invasive traits: a comparative study of invasive and non-invasive heterocarpic Atriplex congeners. PLoS One 12: e0176455. doi: 10.1371/journal.pone.0176455. PubMed DOI PMC

Feng Y, Maurel N, Wang Z, Ning L, Yu FH, van Kleunen M. 2016. Introduction history, climatic suitability, native range size, species traits and their interactions explain establishment of Chinese woody species in Europe. Global Ecology and Biogeography 25: 1356–1366.

Fritz SA, Purvis A. 2010. Selectivity in mammalian extinction risk and threat types: a new measure of phylogenetic signal strength in binary traits. Conservation Biology 24: 1042–1051. PubMed

Fumanal B, Chauvel B, Sabatier A, Bretagnolle F. 2007. Variability and cryptic heteromorphism of Ambrosia artemisiifolia seeds: what consequences for its invasion in France? Annals of Botany 100: 305–313. PubMed PMC

Gioria M, Pyšek P. 2015. The legacy of plant invasions: changes in the soil seed bank of invaded plant communities. BioScience 66: 40–53.

Gioria M, Pyšek P. 2017. Early bird catches the worm: germination as a critical step in plant invasion. Biological Invasions 19: 1055–1080.

Gioria M, Pyšek P, Moravcova L. 2012. Soil seed banks in plant invasions: promoting species invasiveness and long-term impact on plant community dynamics. Preslia 84: 327–350.

Guo WY, van Kleunen M, Winter M, et al. . 2018. The role of adaptive strategies in plant naturalization. Ecology Letters 21: 1380–1389. PubMed

Hannan GL. 1980. Heteromericarpy and dual seed germination modes in Platystemon californicus (Papaveraceae). Madroño 27: 164–170.

Hintze C, Heydel F, Hoppe C, Cunze S, König A, Tackenberg O. 2013. D3: The Dispersal and Diaspore Database – baseline data and statistics on seed dispersal. Perspectives in Plant Ecology, Evolution and Systematics 15: 180–192.

Ho LST, Ané C. 2014. A linear-time algorithm for gaussian and non-gaussian trait evolution models. Systematic Biology 63: 397–408. PubMed

Imbert E. 1999. The effects of achene dimorphism on the dispersal in time and space in Crepis sancta (Asteraceae). Canadian Journal of Botany 77: 508–513.

Imbert E. 2002. Ecological consequences and ontogeny of seed heteromorphism. Perspectives in Plant Ecology Evolution and Systematics 5: 13–36.

Imbert E, Escarre J, Lepart J. 1997. Seed heteromorphism in Crepis sancta (Asteraceae): performance of two morphs in different environments. Oikos 79: 325–332.

Ives A. 2017. R2s for correlated data: phylogenetic models, LMMs, and GLMMs. bioRxiv144170. PubMed

Kalusová V, Chytrý M, van Kleunen M, et al. . 2017. Naturalization of European plants on other continents: the role of donor habitats. Proceedings of the National Academy of Sciences, USA 114: 201705487. PubMed PMC

van Kleunen M, Johnson SD. 2007. South African Iridaceae with rapid and profuse seedling emergence are more likely to become naturalized in other regions. Journal of Ecology 95: 674–681.

van Kleunen M, Richardson DM. 2007. Invasion biology and conservation biology: time to join forces to explore the links between species traits and extinction risk and invasiveness. Progress in Physical Geography 31: 447–450.

van Kleunen M, Dawson W, Schlaepfer D, Jeschke JM, Fischer M. 2010. Are invaders different? A conceptual framework of comparative approaches for assessing determinants of invasiveness. Ecology Letters 13: 947–958. PubMed

van Kleunen M, Dawson W, Essl F, et al. . 2015. Global exchange and accumulation of non-native plants. Nature 525: 100–103. PubMed

van Kleunen M, Bossdorf O, Dawson W. 2018a. The ecology and evolution of alien plants. Annual Review of Ecology, Evolution and Systematics 49: 25–47.

van Kleunen M, Essl F, Perg J, et al. . 2018b. The changing role of ornamental horticulture in alien plant invasions. Biological Reviews 93: 1421–1437. PubMed

Klonner G, Fischer S, Essl F, Dullinger S. 2016. A source area approach demonstrates moderate predictive ability but pronounced variability of invasive species traits. PLoS One 11: e0155547. doi: 10.1371/journal.pone.0155547. PubMed DOI PMC

Kueffer C, Pyšek P, Richardson DM. 2013. Integrative invasion science: model systems, multi-site studies, focused meta-analysis and invasion syndromes. New Phytologist 200: 615–633. PubMed

Kühn I, Durka W, Klotz S. 2004. BiolFlor – a new plant-trait database as a tool for plant invasion ecology. Diversity and Distributions 10: 363–365.

Küster EC, Kühn I, Bruelheide H, Klotz S. 2008. Trait interactions help explain plant invasion success in the German flora. Journal of Ecology 96: 860–868.

Lambdon PW, Pyšek P, Basnou C, et al. . 2008. Alien flora of Europe: species diversity, temporal trends, geographical patterns and research needs. Preslia 80: 101–149.

Lavoie C, Joly S, Bergeron A, Guay G, Groeneveld E. 2016. Explaining naturalization and invasiveness: new insights from historical ornamental plant catalogs. Ecology and Evolution 6: 7188–7198. PubMed PMC

Lei W, Ming D, ZhenYing H. 2010. Review of research on seed heteromorphism and its ecological significance. Journal of Plant Ecology 34: 578–590 [in Chinese].

Maurel N, Hanspach J, Kühn I, Pyšek P, van Kleunen M. 2016. Introduction bias affects relationships between the characteristics of ornamental alien plants and their naturalization success. Global Ecology and Biogeography 25: 1500–1509.

Medvecká J, Kliment J, Májeková J, et al. . 2012. Inventory of the alien flora of Slovakia. Preslia 84: 257–309.

Milbau A, Stout JC. 2008. Factors associated with alien plants transitioning from casual, to naturalized, to invasive. Conservation Biology 22: 308–317. PubMed

Mohamed-Yasseen Y, Barringer SA, Splittstoesser WE, Costanza S. 1994. The role of seed coats in seed viability. The Botanical Review 60: 426–439.

Møller A, Jennions MD. 2002. How much variance can be explained by ecologists and evolutionary biologists? Oecologia 132: 492–500. PubMed

Moravcová L, Pyšek P, Jarošík V, Havlíčková V, Zákravský P. 2010. Reproductive characteristics of neophytes in the Czech Republic: traits of invasive and non-invasive species. Preslia 82: 365–390.

Moravcová L, Pyšek P, Jarošík V, Pergl J. 2015. Getting the right traits: reproductive and dispersal characteristics predict the invasiveness of herbaceous plant species. PLoS One 10: e0123634. doi: 10.1371/journal.pone.0123634. PubMed DOI PMC

Orme D, Freckleton R, Thomas G, et al. . 2013. caper: comparative analyses of phylogenetics and evolution in R.

Pianka ER. 1970. On r- and K-selection. The American Naturalist 104: 592–597.

Plitmann U. 1986. Alternative modes in dispersal strategies, with an emphasis on herbaceous plants of the Middle East. Proceedings of the Royal Society of Edinburgh 89: 193–202.

Prach K, Tichý L, Vítovcová K, Řehounková K. 2017. Participation of the Czech flora in succession at disturbed sites: quantifying species’ colonization ability. Preslia 89: 87–100.

Pyšek P. 1998. Is there a taxonomic pattern to plant invasions? Oikos 82: 282–294.

Pyšek P, Richardson DM. 2007. Traits associated with invasiveness in alien plants: where do we stand? In: Nentwig W, ed. Biological invasions. Berlin, Heidelberg: Springer, 97–125.

Pyšek P, Richardson DM, Williamson M. 2004. Predicting and explaining plant invasions through analysis of source areas floras: some critical considerations. Diversity and Distribution 10: 179–187.

Pyšek P, Jarošík V, Pergl J, et al. . 2009. The global invasion success of Central European plants is related to distribution characteristics in their native range and species traits. Diversity and Distributions 15: 891–903.

Pyšek P, Danihelka J, Sádlo J, et al. . 2012. Catalogue of alien plants of the Czech Republic (2nd edition): checklist update, taxonomic diversity and invasion patterns. Preslia 84: 155–255.

Pyšek P, Manceur AM, Alba C, et al. . 2015. Naturalization of central European plants in North America: species traits, habitats, propagule pressure, residence time. Ecology 96: 762–774. PubMed

Pyšek P, Pergl J, Essl F, et al. . 2017. Naturalized alien flora of the world: species diversity, taxonomic and phylogenetic patterns, geographic distribution and global hotspots of plant invasion. Preslia 89: 203–274.

Rai JPN, Tripathi RS. 1987. Germination and plant survival and growth of Galinsoga parviflora Cav. as related to food and energy content of its ray- and disc-achenes. Acta Oecologica, Oecologia Plantarum 8: 155–165.

Razanajatovo M, Maurel N, Dawson W, et al. . 2016. Plants capable of selfing are more likely to become naturalized. Nature Communications 7: 13313. PubMed PMC

R Core Team 2017. R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.

Reichard SH, White P. 2001. Horticulture as pathways of plant introductions in the United States. BioScience 51: 103–113.

Richardson DM, Pyšek P. 2012. Naturalization of introduced plants: ecological drivers of biogeographical patterns. New Phytologist 196: 383–396. PubMed

Richardson DM, Pyšek P, Rejmánek M, Barbour MG, Panetta FD, West CJ. 2000. Naturalization and invasion of alien plants: concepts and definitions. Diversity and Distributions 6: 93–107.

Richardson DM, Carruthers J, Hui C, et al. . 2011. Human-mediated introductions of Australian acacias – a global experiment in biogeography. Diversity and Distributions 17: 771–787.

Rogerson PA. 2001. Statistical methods for geography. London: Sage Publications Ltd/Cromwell Press Ltd.

Sendek A, Herz K, Auge H, Hensen I, Klotz S. 2015. Performance and responses to competition in two congeneric annual species: does seed heteromorphism matter? Plant Biology 17: 1203–1209. PubMed

Smith SA, Brown JW. 2018. Constructing a broadly inclusive seed plant phylogeny. American Journal of Botany 105: 302–314. PubMed

Tackenberg O. 2003. Modeling long-distance dispersal of plant diaspores by wind. Ecological Monographs 73: 173–189.

Thomson FJ, Moles AT, Auld TD, Kingsford RT. 2011. Seed dispersal distance is more strongly correlated with plant height than with seed mass. Journal of Ecology 99: 1299–1307.

Tutin TG, Heywood VH, Burges NA, et al., eds. 1976. Flora Europaea, Vol. 4. Plantaginaceae to Compositae (and Rubiaceae). Cambridge: Cambridge University Press.

Venable DL. 1985. The evolutionary ecology of seed heteromorphism. The American Naturalist 126: 577–595.

de Waal C, Anderson B, Ellis AG. 2016. Dispersal, dormancy and life-history tradeoffs at the individual, population and species levels in southern African Asteraceae. New Phytologist 210: 356–365. PubMed

Weber EF. 1997. The alien flora of Europe: a taxonomic and biogeographic review. Journal of Vegetation Science 8: 565–572.

Willis SG, Hulme PE. 2004. Environmental severity and variation in the reproductive traits of Impatiens glandulifera. Functional Ecology 18: 887–898.

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...